Med Biol Eng Comput DOI 10.1007/s11517-010-0731-x
ORIGINAL ARTICLE
Impaired gait in ankylosing spondylitis Silvia Del Din • Elena Carraro • Zimi Sawacha Annamaria Guiotto • Lara Bonaldo • Stefano Masiero • Claudio Cobelli
•
Received: 22 June 2010 / Accepted: 26 December 2010 Ó International Federation for Medical and Biological Engineering 2011
Abstract Ankylosing spondylitis (AS) is a chronic, inflammatory rheumatic disease. The spine becomes rigid from the occiput to the sacrum, leading to a stooped position. This study aims at evaluating AS subjects gait alterations. Twenty-four subjects were evaluated: 12 normal and 12 pathologic in stabilized anti-TNF-alpha treatment (mean age 49.42 (10.47), 25.44 (3.19) and mean body mass index 55.75 (3.19), 23.73 (2.7), respectively). Physical examination and gait analysis were performed. A motion capture system synchronized with two force plates was used. Three-dimensional kinematics and kinetics of trunk, pelvis, hip, knee and ankle were determined during gait. A trend towards reduction was found in gait velocity and stride length. Gait analysis results showed statistically
significant alterations in the sagittal plane at each joint for AS patients (P \ 0.049). Hip and knee joint extension moments showed a statistically significant reduction (P \ 0.044). At the ankle joint, a decreased plantarflexion was assessed (P \ 0.048) together with the absence of the heel rocker. Gait analysis, through gait alterations identification, allowed planning-specific rehabilitation intervention aimed to prevent patients’ stiffness together with improve balance and avoid muscles’ fatigue. Keywords Ankylosing spondylitis Kinematics Kinetics Three dimensional Gait analysis
1 Introduction
S. Del Din Z. Sawacha A. Guiotto C. Cobelli (&) Department of Information Engineering, University of Padova, Via Gradenigo 6/B, 35131 Padua, Italy e-mail:
[email protected] S. Del Din e-mail:
[email protected] Z. Sawacha e-mail:
[email protected] A. Guiotto e-mail:
[email protected] E. Carraro L. Bonaldo S. Masiero Department of Rehabilitation Medicine, University of Padova, Via Giustiniani, 2, 35128 Padua, Italy e-mail:
[email protected] L. Bonaldo e-mail:
[email protected] S. Masiero e-mail:
[email protected]
Ankylosing spondylitis (AS) is a chronic, inflammatory rheumatic disease characterised by inflammatory back pain due to sacroiliitis and spondylitis, the formation of syndesmophytes leading to ankylosis, and frequently associated with peripheral arthritis, enthesitis and acute anterior uveitis [31]. AS is thought to be the most common and most typical form of spondyloarthropathy. Spondyloarthropathies usually begin in the late teens and early 20s but may also present earlier in childhood or at an older age; it is very rare for AS to first begin after 45 years of age, but disease is diagnosed at an older age in many patients, in part because symptoms over the years have been minimal [19]. With an estimated prevalence of 0.9% in northern European white populations, AS is a significant health burden to the community [4, 26]. In AS, the spine becomes rigid from the occiput to the sacrum and this leads patients to experience a stooped position. Subjects are unable to see the horizon and experience a shock absorption decrease, which forces them to use a more cautious gait pattern [3].
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Patients with AS could experience a progressive spinal kyphosis, which may induce a forward and downward displacement of the centre of mass (COM) with consequent use of mechanisms to compensate the displacement of the trunk [10]. In these patients, the hip joint does not seem to be involved in their balance control. Thus, it is not involved to compensate a shift of the COM, probably because that these subjects are not able to extend completely the hips when standing. So far in static condition, the compensation may be given by means of knees flexion and ankles plantarflexion as suggested by Bot et al. [3]. Nevertheless the poor posture, decreased range of movement and pain assessed in AS subjects which are commonly associated with balance impairment, caused the need for monitoring the balance impairment in AS patients [22]. Moreover, AS did not show any negative effect on postural stability, indeed the only clinically significant association was found between dynamic postural balance and tragus to wall distance [1]. Even though there is a clinical evidence of an altered posture [1, 3, 22], to our knowledge there are only a few contributions on gait analysis of AS patients [10, 17, 30], and their findings are only related to sagittal joint kinematics, time and space parameters. Zebouni [30] observed decreased range of motion at the hip and knee joints even though no differences in the hip/knee angles ratio with respect to control group were found; in addition, a shorter stride length in AS subjects when compared to controls was noted. Finally, Helliwell [17] observed that AS subjects ‘walked gingerly’. Ankylosing spondylitis is often associated with severe functional impairment, work disability and a compromised quality of life [6, 27], and this calls for a methodology allowing an adequate evaluation of AS motor function, also helping in assessing treatment outcomes. At the best of our knowledge, a complete analysis AS subjects’ motor function based on three-dimensional joint kinematics and kinetics has not been presented. Indeed, nowadays several studies assed the importance of gait analysis in clinical evaluations, in order to provide quantitative evaluation of gait deviations [13, 23]. Thus, the aim of the study was to perform gait analysis of AS patients by means of a protocol already established in our laboratory which evaluates both three-dimensional kinematics and kinetics [20, 25]. An important aspect of our work concerns the study population: patients who are in stabilized anti-TNF-a treatment (i.e. treatment has not been changed at least for about 9 months) which is considered the baseline treatment for reducing the level of pain, stiffness and fatigue [2, 6]. Indeed, common rehabilitation treatments are usually prescribed as a support to the pharmacological therapy to help reducing the level of
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stiffness as well as maintaining good posture and physical, psychological and social functions [6].
2 Methods 2.1 Patients Twenty-four subjects were consecutively enrolled [12 control subjects (CS) and 12 Ankylosing spondylitis (AS)]. AS patients were recruited from the patients attending the outpatient clinic of the Department of Rheumatology of the University of Padova (Italy). Demographic characteristics [sex, age, body mass index (BMI)] and disease characteristics (disease duration, symptoms duration) were obtained. All patients with AS met the most recent modified New York criteria [29] and were eligible to participate in the trial if they were in treatment with standard dose of antiTNF-alfa (Infliximab, 5 mg/kg each 6 weeks) at least from 9 months [5]. Exclusion criteria were of age older than 70 years, concomitant cardiovascular, neurological or psychiatric disease and severe visual or auditory impairments (reduced visual acuity was accepted if adequately corrected). Patients with attested orthopaedic diseases at spine and upper limb (as fracture, spinal disc herniation, spinal surgery, etc.) and lower extremities (as prothesis, osteoarthritis, etc.) were also excluded. The control group consisted of normal subjects enrolled among hospital personnel. The study was approved by the hospital’s ethics committee and informed consent was obtained from all patients and CS. Subjects underwent a morphological examination of the spine using specific assessment tools. The spinal and hip motility of AS patients was evaluated by means of Bath Ankylosing Spondylitis Metrology Index (BASMI) [18] which included the following five measurements: cervical rotation, tragus to wall distance, lumbar side flexion, lumbar flexion and intermalleolar distance. The disease activity was evaluated with the Bath Ankylosing Spondylitis Disease Activity Index (BASDAI) [14] which consists of a one through 100 scale (0 being no problem and 100 being the worst problem). This includes six items pertaining to the five major symptoms of AS: fatigue, spinal pain, joint pain/swelling, areas of localized tenderness (also called enthesitis, or inflammation of tendons and ligaments), morning stiffness duration and morning stiffness severity. The Bath Ankylosing Spondylitis Functional Index (BASFI) was also used for functional ability evaluation, which consists in a self-assessment tool determining how well a patient is currently dealing with AS [7]; BASFI includes eight specific questions regarding function in AS
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and two questions reflecting the patient’s ability to cope with everyday life (consists of a one through 100 scale: 0 being no problem and 100 being the worst problem). 2.2 Instrumentation The instrumental assessment of gait was performed using a six cameras stereophotogrammetric BTS motion capture system (60–120 Hz) synchronized with two Bertec force plates (FP4060-10) and integrated with two Imago S.n.c plantar pressure systems (0.64 cm2 resolution, 150 Hz). A full-body marker set was used [20, 25]: 24 reflective markers were placed on the subjects at anatomical landmarks of head, trunk, thigh, shank, foot, while 24 reflective markers were used for the six clusters (each formed by four markers) of pelvis, thigh and shank (Fig. 1). The following anatomical landmarks were considered for direct marker placement: Trunk
Foot
right and left acromions, spinous process of 7th cervical vertebrae (C7), spinous process of 5th lumbar vertebrae (L5) right and left calcaneus, right and left first metatarsal head, right and left second metatarsal head, right and left fifth metatarsal head
The following anatomical landmarks were considered for direct marker placement and were calibrated with respect to a local cluster of marker by means of a static acquisition: Thigh Shank
right and left lateral and medial epicondyle right and left tibial tuberosity, right and left head of the fibula, right and left lateral and medial malleolus
Four extra markers were applied on the thigh, pelvis and shank in order to create the clusters which were used to calibrate the position of each segment anatomical landmarks [25]. The following anatomical landmarks were calibrated with the aid of a pointer [25]: Pelvis Thigh Shank
right and left anterior superior iliac spine, right and left posterior superior iliac spine right and left greater trochanter right and left tibial tuberosity, right and left head of the fibula, right and left lateral malleolus, right and left medial malleolus
The centre of the femoral head was assumed to coincide with the centre of the acetabulum: the latter was reconstructed by means of a functional method proposed by Cappozzo [8]. Gait was assessed through a static and several dynamic acquisitions. The static acquisition was performed asking the subjects to stand on the compound system comprising both the plantar pressure and force platforms without
Fig. 1 Subject with markers placed according to the adopted protocol, on the left of the figure a frontal view, on the right the lateral view
shoes, with the heels jointed, and with the feet 30° apart [25]. During the dynamic acquisition, the subject was asked to perform independent barefoot gaits by walking along a 10-m walkway, at a self-selected speed, so that the target foot would naturally land on the compound instrument made with both the force and pressure plates. At least three left and right foot strikes were acquired. Anatomical reference frames for the body segments were defined according to previous work [20, 25]. Standard coordinate systems [16] were adopted for each joint, which entails defining flexion/extension as the relative rotation about mediolateral axis of the proximal segment; internal/ external rotation as the relative rotation about the vertical axis of the distal segment; abduction/adduction as the relative rotation about a ‘floating’ axis orthogonal to these two at each collected sample. The joint angles considered for the kinematics analysis were the flexion–extension, abduction–adduction and internal–external rotation of trunk, pelvis, hip and ankle. In particular, when considering the ankle joint, these three rotations were referred to, respectively, as dorsiflexion–plantarflexion, inversion–eversion
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Fig. 2 Gait analysis joint kinematic results. Mean joint angles over the bands of AS subjects (in light gray), of CS (in dark gray) are reported. Horizontal axis depicts one gait cycle; vertical axis represents angles degrees
and internal–external rotation. With respect to the knee in the report of joint rotations, only the flexion–extension angle was reported: abduction–adduction and internal–external rotation were not considered although the model accounts for their values because these joint rotations were not shown to be feasible when reconstructed through markers placed directly on the skin [11, 25]. Joint moments were determined according to Leardini et al. [20]. In the post processing of the kinetics parameters, the flexion–extension, abduction–adduction and internal– external rotation moments of trunk, hip, knees and ankles were considered; together with the medio-lateral, vertical and antero-posterior forces [25]. Joint rotation and moment normative bands (the mean plus and minus one standard deviation) were created using the CS group’s data. The data of the AS groups were compared with them. 2.3 Statistics A t test (Matlab software) was used to compare the AS patients’ and CS’ following variables: age, sex, BMI and time and space parameters (namely: gait velocity, stride period, stride length and stance period).
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Regarding joint rotation angles, moments and forces, each subject’s variables were represented by the mean from three representative walking trials. Intra-class correlation (ICC) was used to aid in selecting each subject’s representative walking trials which could be included in the computation of the mean; thus, the ICC coefficient was calculated for each subject’s kinematic and kinetic parameters. Walking trials whose kinematics or kinetics variables were found with an ICC coefficient less than 0.75 (75%) were excluded from the statistical analysis [21, 25]. The average kinematic and kinetic data, angular displacements and internal joint moments were plotted over one gait cycle (Figs. 2, 3). One-way ANOVA and MANOVA followed by a Tukey–Kramer honestly significant difference post hoc test (Matlab software functions anova1, manova1 and multcompare) were performed between all the AS and CS joint angles and moments in order to compare the AS and CS subjects. The statistical analysis of joint rotation angles was performed relatively to every specific phases of the gait cycle [23]. The statistical analysis of kinetics parameters was performed relatively to every specific phases of the stance phase of gait.
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Fig. 3 Gait analysis joint kinetic results. Mean joint moments over the bands of AS subjects (in light gray), of CS (in dark gray) are reported. Horizontal axis depicts the stance phase; vertical axis represents the percentage of body weight multiplied for height
3 Results The clinical characteristics of the study subjects were reported in Table 1. It can be noticed that baseline demography was comparable between the two groups (Table 1), indeed no significant differences were found considering the age, sex and BMI. In computing the oneway ANOVA between right and left sides biomechanical variables on either the AS subjects or the CS ones, no significant differences were found. So far the mean between the two sides were used in the computation of the mean joint rotations and moments. No significant differences were found between the two groups regarding the following space and time parameters: gait velocity, stride period, stride length and stance period (Table 1). The results of the statistical analysis performed on joint rotations angles and moments together with the ground reaction forces have been reported in Figs. 2, 3, 4 and Table 2. The results of one-way ANOVA and MANOVA statistical analysis on joint rotation angles and moments were expressed with respect to the particular phase of the
gait cycle where significant differences (P \ 0.05) were found between AS and CS groups (Table 2). Ankylosing spondylitis subjects displayed statistically significant increase in trunk extension (0.03 \ P \ 0.03), both hip and knee showed reduction in flexion (0.001 \ P \ 0.049); furthermore, we observed a decreased ankle plantarflexion at initial contact (P = 0.048) and an increased internal rotation (0.014 \ P \ 0.04). Besides, the pelvis rotation angles revealed a statistically significant decrement in the coronal plane (P = 0.04) (see Table 2; Fig. 2). Considering joint rotation moments, they showed a statistically significant reduction in hip and knee joint extension moments during loading response (0.001 \ P \ 0.044) (see Table 2; Fig. 3).
4 Discussion Clinical examination parameters were found in agreement with others [7, 14, 18]. Motor functional and disease activity examination showed that studied subjects had moderate disease, in agreement with Jenkinson’s definition [18] (Table 1).
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Med Biol Eng Comput Table 1 Clinical characteristics, time, and space parameters [mean and standard deviation (SD)] of Ankylosing spondylitis (AS) patients and control subjects (CS) Characteristics
AS Mean (SD)
CS Mean (SD)
P (\0.05)
Age (years)
49.42 (10.47)
55.75 (3.19) 0.058
BMI
25.44 (3.19)
23.73 (2.7)
0.169
Sex
4F/8M
4F/8M
1.00
1.12 (0.25)
0.33
Duration of syntoms (years) 19.92 (8.27) Years of disease (years)
9.17 (6.48)
BASMI
3.38 (1.26)
Cervical rotation (degrees)
104.73 (55.20)
Intermalleoli distance
93.08 (30.16)
Wall-tragus distance
12.88 (4.13)
Schober’s test Lateral inclination
4.14 (1.90) 10.41 (11.46)
BASFI
22.2 (1.32)
BASDAI
25.3 (1.59)
Gait velocity (m/s)
1.05 (0.23)
Stride period (s)
1.19 (0.13)
1.15 (0.05)
0.51
Stride length (m)
0.98 (0.58)
1.29 (0.30)
0.27
Stance period (s)
0.73 (0.08)
0.70 (0.04)
0.65
The reported P values indicate the results of the comparison between the AS and CS groups. A value of P \ 0.05 was considered statistically significant (P*)
With respect to mean joint rotation angles and moments, the results suggested that no significant differences in laterality existed in the analysed subjects. Even though no significant differences were observed in the time and space parameters, a trend towards reduction was found either in the gait velocity or the stride length (see Table 1), as previously reported by Zebouni [30]. These characteristics may indicate that AS patients use a more cautious gait; moreover, the reduced gait velocity together with the shorter stride length could determine an increase in the subject fatigue while walking [28]. The present study showed that the majority of gait alterations were found in the sagittal plane. This could be explained as AS pathology which primarily affects the axial joints leads to biomechanical alterations mostly in this plane. This was found in agreement with previous results about AS postural alteration reported both in clinical examination and static posture analysis [3]. These results lead to the conclusion that AS patients, in order to maintain their balance during gait and cope with a rigid cervical kyphosis, adopt a compensatory strategy: they pivot their trunk around the lumbo-sacral hinge to shift their COM backward. So far, an excessive trunk extension incurred as a result which has been registered during almost the whole gait cycle (namely midstance and swing phase of gait: 10–100% of gait cycle). In addition,
Fig. 4 Gait analysis joint kinetic results. Mean force data over the bands of AS subjects (in light gray), of CS (in dark gray) are reported. Horizontal axis depicts the stance phase; vertical axis represents the percentage of body weight
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Med Biol Eng Comput Table 2 Joint angles and moments range of movement (ROM) [mean and standard deviation (SD)] and one-way ANOVA results for rotation angles and moments during gait computed on the Ankylosing Joint rotations
ROM (°)
spondylitis (AS) group and control subjects (CS) group, respectively, over the phases of the gait cycle and the stance
% of Gait cycle
AS
CS
P value
Mean (SD)
Mean (SD)
0–2%
0–10%
10–30%
30–50%
50–60%
60–73%
73–87%
87–100%
Trunk Flexion/extension
5.84 (1.29)
3.20 (0.91)
ns
ns
0.007*
0.006*
0.030*
0.007*
0.003*
0.018*
Adduction/abduction
10.64 (3.66)
10.60 (3.31)
ns
ns
ns
ns
ns
ns
ns
ns
Internal/external
13.82 (7.25)
12.78 (8.92)
ns
ns
ns
ns
ns
ns
ns
ns
Flexion/extension
34.58 (6.63)
44.50 (3.90)
0.004*
0.007*
0.002*
ns
ns
ns
0.049*
0.001*
Adduction/abduction
14.97 (5.26)
11.89 (3.79)
ns
ns
ns
ns
ns
ns
ns
0.033*
Internal/external
15.95 (8.73)
14.04 (5.19)
ns
ns
ns
ns
ns
ns
ns
ns
Hip
Pelvis Tilt Obliquity Rotation
4.64 (1.61)
2.72 (2.10)
ns
ns
ns
ns
ns
ns
ns
ns
7.60 (3.91) 11.17 (9.14)
6.74 (1.47) 7.40 (3.46)
ns ns
ns ns
ns ns
0.040* ns
ns ns
ns ns
ns ns
ns ns
65.49 (7.58)
64.54 (7.61)
0.046
0.037
0.031
ns
ns
ns
0.021*
0.011*
Knee Flexion/extension Ankle Dorsiflexion/plantarflexion
29.28 (8.11)
29.02 (5.71)
0.048*
ns
ns
ns
ns
ns
ns
ns
Eversion/inversion
12.11 (2.22)
13.80 (3.70)
ns
ns
ns
ns
ns
ns
ns
ns
Internal/external
13.93 (5.41)
10.02 (1.96)
ns
ns
0.031*
ns
ns
ns
0.014*
0.040*
Joint moments
% of BW 9 H
% of Stance
AS
CS
P value
Mean (SD)
Mean (SD)
0–3.33%
0–16.67%
16.67–50%
50–83.33%
83.33–100%
Extension/flexion
9.40 (4.67)
8.92 (3.45)
ns
ns
ns
0.028*
0.002*
Abduction/adduction
2.01 (0.65)
2.10 (0.42)
0.004*
0.013*
0.042*
ns
0.008*
External/internal
1.68 (0.95)
1.80 (2.75)
ns
ns
ns
ns
ns
Extension/flexion
5.97 (3.56)
7.71 (2.28)
0.044*
ns
ns
ns
ns
Abduction/adduction External/internal
5.00 (0.60) 0.91 (0.26)
5.35 (2.02) 1.59 (2.15)
ns 0.006*
ns 0.006*
0.013* 0.009*
0.003* 0.016*
0.006* 0.029*
Extension/flexion
4.16 (1.56)
3.74 (1.71)
ns
0.005*
0.000*
0.001*
ns
Valgus/varus
2.50 (0.78)
2.30 (0.79)
ns
ns
ns
ns
ns
External/internal
0.63 (0.32)
0.78 (0.78)
0.000*
0.001*
ns
ns
ns
Trunk
Hip
Knee
Ankle Plantarflexion/dorsiflexion
8.71 (0.64)
6.99 (2.11)
0.001*
0.000*
0.036*
ns
0.004*
Eversion/inversion
1.62 (0.39)
1.36 (0.41)
ns
ns
ns
ns
ns
External/internal
1.55 (0.59)
2.76 (1.52)
ns
ns
0.000*
0.000*
0.000*
A value of P \ 0.05 was considered statistically significant. ns non-significant, P* indicate results of the comparison between the AS and CS groups
the pelvis rotation angles revealed a statistically significant difference in the coronal plane (pelvis obliquity) which was found decreased in the terminal stance (30–50% of the gait
cycle) phase of gait, in agreement with the rigidity of AS patients described by [3]. Moreover, this reduction in pelvic oscillation can reduce subject stability during gait.
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In this study, when considering both the trunk flexion/ extension angle and the pelvic tilt, a pattern similar to a double bump can be noticed, which could be interpreted as a strategy to cope with poor balance due to a forward shift of the centre of mass. Nevertheless, both hip and knee showed reduction in flexion during the loading response and the last two phases of the gait cycle. These alterations were found in agreement with joint rotation moments which showed a statistically significant reduction in hip and knee joint extension moments during loading response. Furthermore, a decreased ankle plantarflexion was assessed at initial contact. In contrast with the CS group, a dorsiflexion moment was registered at heel strike, together with an excessive posterior force which lead to lower gait velocity, shorter stride length during gait, as well as lower vertical force during stance. So far, AS subjects experienced difficulties in the step negotiation at the beginning of the gait cycle. These biomechanical alterations in the sagittal plane could explain the lack of heel rocker due to difficulties in accomplishing the shock absorption. This was in agreement with a previous study which related the reduced shock absorption of AS patients to the rigidity of the spine [17]. Furthermore, AS subjects exhibited lower gait patterns variability when compared with control group, which seemed to display the presence of a homogeneous and well-established gait pattern in these subjects, probably due to a rigidity of the spine which is a typical characteristic of these subjects. Their tissue is gradually replaced by fibrocartilage and then becomes ossified; moreover, in advanced stages of the disease, the fusion typically ascends the spine, forming a long bony column referred to as ‘bamboo spine’. Our results seem to suggest the presence of a homogeneous and well-established gait pattern in these subjects, which we associated with the rigidity of the spine which is a typical characteristic of this pathology. So far, we could speculate whether these subjects would not change their gait pattern with the progression of the disease, which leads to the fusion of the spine. However, further study should be performed on a larger sample subjects in order to confirm this hypothesis. The alterations highlighted in the present paper outlined a patient with problems of rigidity and balance impairments not only displayed in static condition (as reported by [3, 22]) but also during gait. Nowadays, AS patients rehabilitation programs aim at preventing AS patient stiffness through increasing their limited ROM and improving their muscle stretching [31]. Based on the results of the present paper, an efficient rehabilitation treatment should further include specific proprioceptive exercise to improve AS balance and specific training exercise to avoid muscle fatigue.
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With regards to the instrumental setup, in this study, a stereophotogrammetric system was adopted for its ability to determine lower limb and trunk three-dimensional joint kinematics. Alternative methods based on wearable inertial and magnetic measurement systems such as three-dimensional accelerometers, gyroscopes and magnetometers could have also been adopted [9, 12, 15]. However, to the author knowledge only two works have been published reporting the joint angular kinematics of hip, knee and ankle, during upright posture and during level walking [9, 24]. In both cases [9, 24] the trunk kinematic was not determined, and in one of them the protocol requires for each body segment to establish the orientation of a minimum of two non-parallel lines using multiple calibration tasks, involving multiple specialized devices at the expense of simplicity and experiment duration [9]. In this context, it should be mentioned that AS pathology mostly affects the spine, so far a protocol suitable for evaluating AS subjects kinematics during gait should be able to estimate the threedimensional trunk kinematics. Results of the present study assessed the ability of gait analysis in describing AS subject gait impairments, thus allowing to plan specific rehabilitation interventions for this type of patients. Acknowledgments The authors thank the contribution of Roberta Guglielmin and Mariangela Sambini for their help in collecting the clinical data on AS patients.
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